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Maternal effects and fitness associated
recombination in a host-pathogen
system
Weihao Zhong
Nicholas Priest
07/01/2012
Rutherford & Lindquist (1998) Nature 396, 336-342
McClintock (1984) Science 226, 792-801
Stress
Increased
phenotypic
variation
Increased
genetic
variation
Stress-induced GV:
- Increase the total additive GV available for selection
- Suggest a plausible mechanism for the evolution of sex &
recombination
The problem with recombination
• Recombination load
– “The Reduction Principle” (Feldman et al.
1980)
• Recombination evolves under limited
conditions in classic models
– e.g. weak negative epistasis
• But, a constant rate of recombination is
assumed
Recombination as a plastic trait
• Numerous examples of stress-induced
recombination
– Temperature (Plough 1917; Grell 1971;
Zhong & Priest 2011)
– Nutrition (Neel 1941)
– Mating (Priest et al. 2007; Stevison 2011)
– Introduction of deleterious mutations
(Tedman-Aucoin & Agrawal 2011)
Meiotic recombination is a plastic trait that is sensitive
to physiological state of the organism.
Fitness-Associated Recombination
• FAR modifiers evolve under
broad range of conditions
(Hadany & Beker 2003):
– Form direct association with
locus under selection
– No epistasis required
• Require maternal effect on
recombination to work in
diploids (Agrawal et al. 2005)
Recombination
Fitness
RecombinationOffspringMother
Stress
Are stress-induced maternal effects
common in nature? Yes!
Tenebrio molitor Tribolium castaneum
Bombus terrestris
Porcellio scaber
Daphnia magna Plodia interpunctella
“Trans-generational immune priming”
1. Does maternal stress affect offspring
recombination?
2. Is there a negative relationship between
fitness and recombination?
Testing them requires multi-generation experiments
with biologically realistic stress that assess direct
correlation between fitness and recombination.
• Backcross phenotypic markers
• Create heterozygous females, tester male mating
• Score Non-recombinants Recombinants
A B
B
A
X
XWT XWT
A B
Multiple
Generations General approach
Maternal
Generation
Daughter
Generation
NT+NT
NT+ME
ME+NT
ME+ME
Offspring Scoring
Live pathogen Heat-killed pathogen
Back-crossed marker line
OR
NT ME
OR
Daughters collected
NT ME
Daughters collected
Offspring Scoring
OR
OR
NT+NT
NT+HT
HT+NT
HT+HT
NT HT
NT HT
Metarhizium robertsii
No maternal effect on reproductive output
NT+NT NT+ME ME+NT ME+ME
Totalscored
010203040506070
a a
b b
77 73 72 64
Maternal: F1,282 = 0.59, p = 0.44
Daughter: F1,282 = 31.2, p < 0.001
Maternal x Daughter: F1,282 = 0.01, p = 0.93
Mother
Daughter
NT+NT NT+HT HT+NT HT+HT
Totalscored
010203040506070
b
a a
a
77 65 73 65
Maternal: F1,276 = 0.82, p = 0.37
Daughter: F1,276 = 3.5, p = 0.05
Maternal x Daughter: F1,276 = 1.45, p = 0.23
Mother
Daughter
“Pathogen exposure enhances host
fitness” - Colin McClure (C15, Friday
@ 11.20)
Maternal effect on recombination
NT+NT NT+ME ME+NT ME+ME
Recombinationrate(cM/Mb)
0.00.51.01.52.02.53.03.5
65 38 59 37
a a a a
Maternal: χ2 = 0.15, p = 0.70
Daughter: χ2 = 0.33, p = 0.57
Maternal x Daughter: χ2 = 0.01, p = 0.94
NT+NT NT+HT HT+NT HT+HT
Recombinationrate(cM/Mb)
0.00.51.01.52.02.53.03.5
65 67 53 55
a a a
b
Maternal: χ2 = 3.8, p = 0.05
Daughter: χ2 = 0.62, p = 0.43
Maternal x Daughter: χ2 = 5.2, p < 0.05
Mother
Daughter
Mother
Daughter
No correlation between recombination
& reproductive output
20 40 60 80 100
123456
NT+NT
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
1234
NT+HT
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
1.01.52.02.53.03.54.0
NT+ME
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80
2345
ME+ME
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
1234
HT+NT
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
2345
ME+NT
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
12345
HT+HT
Number of Offspring Scored
RateofRecombination(cM/Mb)
20 40 60 80 100
0123
HT+ME
Number of Offspring Scored
RateofRecombination(cM/Mb)
All p > 0.05
Results
1. Does maternal stress affect offspring
recombination?
2. Is there a negative relationship between
fitness and recombination?
- Live pathogen
- Heat-killed pathogen
- Stress treatment
- Control
Implications
• Fitness Associated Recombination might be
relatively rare in nature (in Diploids)
– Weaker association between modifier and selected
loci
• Maternal ‘priming’ effects can have unexpected
consequences
– Interaction between maternal cues (past stress
exposure) and offspring stress (current exposure)
– Do populations possess stress ‘memory’?
Take-home message
The effects of stress on genetic variation
extend beyond a single generation…
…though exposure to stress does not
always increase the genetic potential for
adaptation.
Acknowledgements
Nicholas Priest
Colin McClure
James Sciberras
Dave Mlynski

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Zhong Nottingham Jan 2012 [FINAL]

  • 1. Maternal effects and fitness associated recombination in a host-pathogen system Weihao Zhong Nicholas Priest 07/01/2012
  • 2. Rutherford & Lindquist (1998) Nature 396, 336-342 McClintock (1984) Science 226, 792-801 Stress Increased phenotypic variation Increased genetic variation Stress-induced GV: - Increase the total additive GV available for selection - Suggest a plausible mechanism for the evolution of sex & recombination
  • 3. The problem with recombination • Recombination load – “The Reduction Principle” (Feldman et al. 1980) • Recombination evolves under limited conditions in classic models – e.g. weak negative epistasis • But, a constant rate of recombination is assumed
  • 4. Recombination as a plastic trait • Numerous examples of stress-induced recombination – Temperature (Plough 1917; Grell 1971; Zhong & Priest 2011) – Nutrition (Neel 1941) – Mating (Priest et al. 2007; Stevison 2011) – Introduction of deleterious mutations (Tedman-Aucoin & Agrawal 2011) Meiotic recombination is a plastic trait that is sensitive to physiological state of the organism.
  • 5. Fitness-Associated Recombination • FAR modifiers evolve under broad range of conditions (Hadany & Beker 2003): – Form direct association with locus under selection – No epistasis required • Require maternal effect on recombination to work in diploids (Agrawal et al. 2005) Recombination Fitness RecombinationOffspringMother Stress
  • 6. Are stress-induced maternal effects common in nature? Yes! Tenebrio molitor Tribolium castaneum Bombus terrestris Porcellio scaber Daphnia magna Plodia interpunctella “Trans-generational immune priming”
  • 7. 1. Does maternal stress affect offspring recombination? 2. Is there a negative relationship between fitness and recombination? Testing them requires multi-generation experiments with biologically realistic stress that assess direct correlation between fitness and recombination.
  • 8. • Backcross phenotypic markers • Create heterozygous females, tester male mating • Score Non-recombinants Recombinants A B B A X XWT XWT A B Multiple Generations General approach
  • 9. Maternal Generation Daughter Generation NT+NT NT+ME ME+NT ME+ME Offspring Scoring Live pathogen Heat-killed pathogen Back-crossed marker line OR NT ME OR Daughters collected NT ME Daughters collected Offspring Scoring OR OR NT+NT NT+HT HT+NT HT+HT NT HT NT HT Metarhizium robertsii
  • 10. No maternal effect on reproductive output NT+NT NT+ME ME+NT ME+ME Totalscored 010203040506070 a a b b 77 73 72 64 Maternal: F1,282 = 0.59, p = 0.44 Daughter: F1,282 = 31.2, p < 0.001 Maternal x Daughter: F1,282 = 0.01, p = 0.93 Mother Daughter NT+NT NT+HT HT+NT HT+HT Totalscored 010203040506070 b a a a 77 65 73 65 Maternal: F1,276 = 0.82, p = 0.37 Daughter: F1,276 = 3.5, p = 0.05 Maternal x Daughter: F1,276 = 1.45, p = 0.23 Mother Daughter “Pathogen exposure enhances host fitness” - Colin McClure (C15, Friday @ 11.20)
  • 11. Maternal effect on recombination NT+NT NT+ME ME+NT ME+ME Recombinationrate(cM/Mb) 0.00.51.01.52.02.53.03.5 65 38 59 37 a a a a Maternal: χ2 = 0.15, p = 0.70 Daughter: χ2 = 0.33, p = 0.57 Maternal x Daughter: χ2 = 0.01, p = 0.94 NT+NT NT+HT HT+NT HT+HT Recombinationrate(cM/Mb) 0.00.51.01.52.02.53.03.5 65 67 53 55 a a a b Maternal: χ2 = 3.8, p = 0.05 Daughter: χ2 = 0.62, p = 0.43 Maternal x Daughter: χ2 = 5.2, p < 0.05 Mother Daughter Mother Daughter
  • 12. No correlation between recombination & reproductive output 20 40 60 80 100 123456 NT+NT Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 1234 NT+HT Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 1.01.52.02.53.03.54.0 NT+ME Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 2345 ME+ME Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 1234 HT+NT Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 2345 ME+NT Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 12345 HT+HT Number of Offspring Scored RateofRecombination(cM/Mb) 20 40 60 80 100 0123 HT+ME Number of Offspring Scored RateofRecombination(cM/Mb) All p > 0.05
  • 13. Results 1. Does maternal stress affect offspring recombination? 2. Is there a negative relationship between fitness and recombination? - Live pathogen - Heat-killed pathogen - Stress treatment - Control
  • 14. Implications • Fitness Associated Recombination might be relatively rare in nature (in Diploids) – Weaker association between modifier and selected loci • Maternal ‘priming’ effects can have unexpected consequences – Interaction between maternal cues (past stress exposure) and offspring stress (current exposure) – Do populations possess stress ‘memory’?
  • 15. Take-home message The effects of stress on genetic variation extend beyond a single generation… …though exposure to stress does not always increase the genetic potential for adaptation.